Correlative adaptation between Rubisco and CO2-concentrating mechanisms in seagrasses

Submerged angiosperms sustain some of the most productive and diverse ecosystems worldwide. However, their carbon acquisition and assimilation mechanisms remain poorly explored, missing an important step in the evolution of photosynthesis during the colonization of aquatic environments by angiosperms. Here we reveal a convergent kinetic adaptation of Rubisco in phylogenetically distant seagrass species that share catalytic efficiencies and CO2 and O-2 affinities up to three times lower than those observed in phylogenetically closer angiosperms from terrestrial, freshwater and brackish-water habitats. This Rubisco kinetic convergence was found to correlate with the effectiveness of seagrass CO2-concentrating mechanisms (CCMs), which probably evolved in response to the constant CO2 limitation in marine environments. The observed Rubisco kinetic adaptation in seagrasses more closely resembles that seen in eukaryotic algae operating CCMs rather than that reported in terrestrial C-4 plants. Our results thus demonstrate a general pattern of co-evolution between Rubisco function and biophysical CCM effectiveness that traverses distantly related aquatic lineages. Rubisco in seagrasses converged on lower catalytic efficiencies and CO2/O-2 affinities than in their terrestrial and freshwater relatives, as a result of correlative adaptation between Rubisco and the effectiveness of their CO2-concentrating mechanisms.